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Genome-wide rotational and translational phasing of nucleosomes with human transcription factors

ABSTRACT: How transcription factors (TFs) and their binding sites organize and engage nucleosomes at natural genomic locations remains poorly understood. Here we develop Benzonase-seq to measure the rotational phasing of nucleosomes in human cells, and enhance ChIP-exo (v6) to measure rotational phasing on the same DNA molecule bound by a TF. Unbound CTCF sites were found to be rotationally accessible on nucleosomes and this rotational accessibility is encoded by classical dinucleotide periodicities. CTCF binding results in nucleosome displacement to adjacent DNA phasing sequences. Examining 40 TF classes, their unbound sites were phased inward, outward, or lacked phasing. In all examined cases, TF binding (e.g. NFIA and FoxA) results in adjacent rotational and translational phasing, which is not dinucleotide encoded. Benzonase-seq also more robustly maps nucleosome and subnucleosome positions in hard-to-map CpG islands. These findings provide a clearer view of how TFs engage and position nucleosomes to shape the natural chromatin landscape.

ORGANISM(S): Homo sapiens

PROVIDER: GSE267711 | GEO | 2026/07/02

REPOSITORIES: GEO

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Genome-wide rotational and translational phasing of nucleosomes with human transcription factors

Project description:How transcription factors (TFs) and their binding sites organize and engage nucleosomes at natural genomic locations remains poorly understood. Here we develop Benzonase-seq to measure the rotational phasing of nucleosomes in human cells, and enhance ChIP-exo (v6) to measure rotational phasing on the same DNA molecule bound by a TF. Unbound CTCF sites were found to be rotationally accessible on nucleosomes and this rotational accessibility is encoded by classical dinucleotide periodicities. CTCF binding results in nucleosome displacement to adjacent DNA phasing sequences. Examining 40 TF classes, their unbound sites were phased inward, outward, or lacked phasing. In all examined cases, TF binding (e.g. NFIA and FoxA) results in adjacent rotational and translational phasing, which is not dinucleotide encoded. Benzonase-seq also more robustly maps nucleosome and subnucleosome positions in hard-to-map CpG islands. These findings provide a clearer view of how TFs engage and position nucleosomes to shape the natural chromatin landscape.

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Project description:Mammalian gene expression is controlled by transcription factors (TFs) that engage sequence motifs in a chromatinized genome, where nucleosomes can restrict DNA access. Yet, how nucleosomes affect individual TFs remains unclear. Here, we measure the ability of over one hundred TF motifs to recruit TFs in a defined chromosomal locus in mouse embryonic stem cells. This identifies a set sufficient to enable binding of TFs with diverse tissue specificities, functions, and DNA binding domains. These chromatin-competent factors are further classified when challenged to engage motifs within a highly-phased nucleosome. The pluripotency factors OCT4- SOX2 preferentially engage non-nucleosomal and entry-exit motifs, but not nucleosome internal sites, a preference that also guides binding genome-wide. By contrast, factors such as BANP, REST, or CTCF, engage throughout causing nucleosomal displacement.This reveals that TFs vary widely in their sensitivity to nucleosomes and that genome access is TF-specific and influenced by nucleosome position in the cell.

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Genome-wide rotational and translational phasing of nucleosomes with human transcription factors [ChIP-exo]

Project description:Eukaryotic DNA is wrapped around a complex of histones, such that one face of the helix is accessible, and the other is buried. Sliding and rotating DNA by 5 bp in either direction reverses this polarity. This has substantial ramifications for regulating transcription factor (TF) binding. Yet, there does not exist a method to measure the rotational setting of DNA on nucleosomes in vivo and on a genomic scale. We developed Benzonase-seq, Benzonase cleaves and marks the accessible rotationally exposed DNA surface, in addition to marking linker regions between nucleosomes. Further, Benzonase robustly maps nucleosomes in CpG-rich mammalian promoters compared, which has been challenging for the commonly used micrococcal nuclease (MNase). When Benzonase cleavages are analyzed in the context of TF binding sites, we determine whether the TF motif has a prefer orientation on the nucleosome surface. When this assay is coupled to chromatin immunoprecipitation (ChIP) of histones, histone variants, and modifications, we find evidence for transcription-linked subnucleosomal structures, some of which may be related to hexasomes and half/split-nucleosomes. Benzonase-seq offers a robust and ultra-high resolution method to map the translational and rotational setting of DNA elements on the nucleosome surface, and provides a means to probe subnucleosomal structures. Benzonase-seq may be useful for probing the pioneering potential of transcription factors.

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The CentO satellite confers translational and rotational phasing on cenH3 nucleosomes in rice centromeres

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Oryza sativa

Project description:The CentO satellite confers translational and rotational phasing on cenH3 nucleosomes in rice centromeres

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